Skip to main content

Food sources used by sediment meiofauna in an intertidal Zostera noltii seagrass bed: a seasonal stable isotope study

Marine Biology volume 159, pages 1537–1550 (2012)Cite this article

Abstract

In an intertidal Zostera noltii Hornem seagrass bed, food sources used by sediment meiofauna were determined seasonally by comparing stable isotope signatures (δ13C, δ15N) of sources with those of nematodes and copepods. Proportions of different carbon sources used by consumers were estimated using the SIAR mixing model on δ13C values. Contrary to δ15N values, food source mean δ13C values encompassed a large range, from −22.1 ‰ (suspended particulate organic matter) to −10.0 ‰ (Z. noltii roots). δ13C values of copepods (from −22.3 to −12.3 ‰) showed that they use many food sources (benthic and phytoplanktonic microalgae, Z. noltii matter). Nematode δ13C values ranged from −14.6 to −11.4 ‰, indicating a strong role of microphytobenthos and/or Z. noltii matter as carbon sources. The difference of food source uses between copepods and nematodes is discussed in light of source accessibility and availability.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  • Anesio AM, Abreu PC, Biddanda BA (2003) The role of free and attached microorganisms in the decomposition of estuarine macrophyte detritus. Estuar Coast Shelf Sci 56:197–201

    Article  Google Scholar 

  • Asmus H, Asmus R (1985) The importance of grazing food chain for energy flow and production in three intertidal sand bottom communities of the northern Wadden Sea. Helgol Meeresunters 39:273–301

    Article  Google Scholar 

  • Bell SS, Walters K, Kern JC (1984) Meiofauna from seagrass habitats: a review and prospectus for future research. Estuaries 7:331–338

    Article  Google Scholar 

  • Benner R, Fogel ML, Sprague EK, Hodson RE (1987) Depletion of 13C in lignin and its implication for stable carbon isotope studies. Nature 329:708–710

    Article  CAS  Google Scholar 

  • Borowitzka MA, Lavery PS, van Keulen M (2006) Epiphytes of seagrasses. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 441–461

    Chapter  Google Scholar 

  • Boschker HTS, Wielemaker A, Schaub BEM, Holmer M (2000) Limited coupling of macrophyte production and bacterial carbon cycling in the sediments of Zostera spp. meadows. Mar Ecol Prog Ser 203:181–189

    Article  CAS  Google Scholar 

  • Buffan-Dubau E, Castel J (1996) Diel and seasonal vertical distribution of meiobenthic copepods in muddy sediments of a eutrophic lagoon (fish ponds of Arcachon Bay). Hydrobiologia 329:69–78

    Article  CAS  Google Scholar 

  • Buffan-Dubau E, de Wit R, Castel J (1996) Feeding selectivity of the harpacticoid copepod Canuella perplexa in benthic muddy environments demonstrated by HPLC analyses of chlorin and carotenoid pigments. Mar Ecol Prog Ser 137:71–82

    Article  CAS  Google Scholar 

  • Burgess R (2001) An improved protocol for separating meiofauna from sediments using colloidal silica sols. Mar Ecol Prog Ser 214:161–165

    Article  Google Scholar 

  • Carman KR, Fry B (2002) Small-sample methods for δ13C and δ15N analysis of the diets of marsh meiofaunal species using natural-abundance and tracer-addition isotope techniques. Mar Ecol Prog Ser 240:85–92

    Article  CAS  Google Scholar 

  • Castel J, Labourg P-J, Escavarage V, Auby I, García ME (1989) Influence of seagrass beds and oyster parks on the abundance and biomass patterns of meio- and macrobenthos in tidal flats. Estuar Coast Shelf Sci 28:71–85

    Article  Google Scholar 

  • Cebrián J (1999) Patterns in the fate of production in plant communities. Am Nat 154:449–468

    Article  Google Scholar 

  • Coull BA (1999) Role of meiofauna in estuarine soft-bottom habitats. Aust J Ecol 24:327–343

    Article  Google Scholar 

  • Daehnick AE, Sullivan MJ, Moncreiff CA (1992) Primary production of the sand microflora in seagrass beds of Mississipi Sound. Bot Mar 35:131–139

    Google Scholar 

  • Danovaro R (1996) Detritus-bacteria-meiofauna interactions in a seagrass bed (Posidonia oceanica) of the NW Mediterranean. Mar Biol 127:1–13

    Article  CAS  Google Scholar 

  • Danovaro R, Gambi C (2002) Biodiversity and trophic structure of nematode assemblages in seagrass systems: evidence for a coupling with changes in food availability. Mar Biol 141:667–677

    Article  CAS  Google Scholar 

  • Danovaro R, Gambi C, Mirto S (2002) Meiofaunal production and energy transfer efficiency in a seagrass Posidonia oceanica bed in the western Mediterranean. Mar Ecol Prog Ser 234:95–104

    Article  Google Scholar 

  • de Jonge VN (1979) Quantitative separation of benthic diatoms from sediments using density gradient centrifugation in the colloidal silica Ludox-TM. Mar Biol 51:267–278

    Article  Google Scholar 

  • De Troch M, Gurdebeke S, Fiers F, Vincx M (2001) Zonation and structuring factors of meiofauna communities in a tropical seagrass bed (Gazi Bay, Kenya). J Sea Res 45:45–61

    Article  Google Scholar 

  • De Troch M, Fiers F, Vincx M (2003) Niche segregation and habitat specialisation of harpacticoid copepods in a tropical seagrass bed. Mar Biol 142:345–355

    Google Scholar 

  • De Troch M, Houthoofd L, Chepurnov VA, Vanreusel A (2006) Does sediment grain size affect diatom grazing by harpacticoid copepods? Mar Environ Res 61:265–277

    Article  Google Scholar 

  • Dechambenoy CL, Pontier F, Sirou F, Vouvé J (1977) Apport de la thermographie infrarouge aéroportée à la connaissance de la dynamique superficielle des estuaires (système Charente-Seudre-Anse de l’Aiguillon). CR Acad Sci Paris 284:1269–1272

    Google Scholar 

  • Dijkstra P, LaViolette CM, Coyle JS, Doucett RR, Schwartz E, Hart SC, Hungate BA (2008) 15N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function. Ecol Lett 11:389–397

    Article  Google Scholar 

  • Duarte CM (1989) Temporal biomass variability and production/biomass relationships of seagrass communities. Mar Ecol Prog Ser 51:269–276

    Article  Google Scholar 

  • Duarte CM, Cebrián J (1996) The fate of marine autotrophic production. Limnol Oceanogr 41:1758–1766

    Article  CAS  Google Scholar 

  • Duarte CM, Chiscano CL (1999) Seagrass biomass and production: a reassessment. Aquat Bot 65:159–174

    Article  Google Scholar 

  • Edwards W, Lindman A, Savage LJ (1963) Bayesian statistical inference in statistical research. Psychol Res 70:193–242

    Google Scholar 

  • Escavarage V, García ME, Castel J (1989) The distribution of meiofauna and its contribution to detritic pathways in tidal flats (Arcachon Bay, France). Sci Mar 53:551–559

    Google Scholar 

  • Findlay S, Tenore K (1982) Nitrogen source for a detritivore: detritus substrate versus associated microbes. Science 218:371–373

    Article  CAS  Google Scholar 

  • Fonseca G, Hutchings P, Gallucci F (2011) Meiobenthic communities of seagrass beds (Zostera capricorni) and unvegetated sediments along the coast of New South Wales, Australia. Estuar Coast Shelf Sci 91:69–77

    Article  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • Galois R, Richard P, Fricourt B (1996) Seasonal variations in suspended particulate matter in the Marennes-Oléron Bay, France, using lipids as biomarkers. Estuar Coast Shelf Sci 43:335–357

    Article  CAS  Google Scholar 

  • Giere O (2009) Meiobenthology. The microscopic motile fauna of aquatic sediments, 2nd edn. Springer, Berlin, pp XVII–527

  • Giraudoux P (2011) Pgirmess: data analysis in ecology. R package version 1.5.0. http://cran.r-project.org/web/packages/pgirmess/index.html

  • Guillaumont B (1991) Utilisation de l’imagerie satellitaire pour des comparaisons spatiales et temporelles en zone intertidale. In: Elliott M, Ducrotoy J-P (eds) Estuaries and coasts: spatial and temporal intercomparisons. ECSA19 symposium. Olsen & Olsen, Fredensborg, pp 63–68

  • Heip C, Vincx M, Vranken G (1985) The ecology of marine nematodes. Oceanogr Mar Biol Annu Rev 23:399–489

    Google Scholar 

  • Herlory O, Richard P, Blanchard GF (2007) Methodology of light response curves: application of chlorophyll fluorescence to microphytobenthic biofilms. Mar Biol 153:91–101

    Article  CAS  Google Scholar 

  • Hicks GRF, Coull BC (1983) The ecology of marine meiobenthic harpacticoid copepods. Oceanogr Mar Biol Annu Rev 21:67–175

    Google Scholar 

  • Holmer M, Duarte CM, Boschker HTS, Barrón C (2004) Carbon cycling and bacterial carbon sources in pristine and impacted Mediterranean seagrass sediments. Mar Ecol Prog Ser 36:227–237

    Google Scholar 

  • Hyndes GA, Lavery PS (2005) Does transported seagrass provide an important trophic link in unvegetated, nearshore areas? Estuar Coast Shelf Sci 63:633–643

    Article  CAS  Google Scholar 

  • Kaldy JE, Onuf CP, Eldridge PM, Cifuentes LA (2002) Carbon budget for a subtropical seagrass dominated coastal lagoon: how important are seagrasses to total ecosystem net primary production? Estuaries 25:528–539

    Article  CAS  Google Scholar 

  • Kang CK, Sauriau P-G, Richard P, Blanchard GF (1999) Food sources of the infaunal suspension-feeding bivalve Cerastoderma edule in a muddy sandflat of Marennes-Oléron Bay, as determined by analyses of carbon and nitrogen stable isotopes. Mar Ecol Prog Ser 187:147–158

    Article  Google Scholar 

  • Kharlamenko VI, Kiyashko SI, Rodkina SA, Imbs AB (2008) Determination of food sources of marine invertebrates from a subtidal sand community using analyses of fatty acids and stable isotopes. Russ J Mar Biol 34:101–109

    Article  CAS  Google Scholar 

  • Koch EW, Ackerman JD, Verduin J, van Keulen M (2006) Fluid dynamics in seagrass ecology—from molecules to ecosystems. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 193–225

    Chapter  Google Scholar 

  • Lebreton B, Richard P, Radenac G, Bordes M, Bréret M, Arnaud C, Mornet F, Blanchard GF (2009) Are epiphytes a significant component of intertidal Zostera noltii beds? Aquat Bot 91:82–90

    Article  Google Scholar 

  • Lebreton B, Richard P, Galois R, Radenac G, Pfléger C, Guillou G, Mornet F, Blanchard GF (2011) Trophic importance of diatoms in an intertidal Zostera noltii seagrass bed: evidence from stable isotope and fatty acid analyses. Estuar Coast Shelf Sci 92:140–153

    Article  CAS  Google Scholar 

  • Leduc D, Probert PK (2011) Small-scale effect of intertidal seagrass (Zostera muelleri) on meiofaunal abundance, biomass, and nematode community structure. J Mar Biol Ass UK 91:579–591

    Article  Google Scholar 

  • Leduc D, Probert PK, Frew RD, Hurd CL (2006) Macroinvertebrate diet in intertidal seagrass and sandflat communities: a study using C, N, and S stable isotopes. N Z J Mar Freshw Res 40:615–629

    Article  CAS  Google Scholar 

  • Leduc D, Probert PK, Duncan A (2009) A multi-method approach for identifying meiofaunal trophic connections. Mar Ecol Prog Ser 383:95–111

    Article  CAS  Google Scholar 

  • Moens T, Vincx M (1997) Observations on the feeding ecology of estuarine nematodes. J Mar Biol Ass UK 77:211–227

    Article  Google Scholar 

  • Moens T, Luyten C, Middelburg JJ, Herman PMJ, Vincx V (2002) Tracing organic matter sources of estuarine tidal flat nematodes with stable carbon isotopes. Mar Ecol Prog Ser 234:127–137

    Article  Google Scholar 

  • Moens T, Bouillon S, Gallucci F (2005) Dual stable isotope abundances unravel trophic position of estuarine nematodes. J Mar Biol Ass UK 85:1401–1407

    Article  CAS  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672. doi:10.1371/journal.pone.0009672

    Article  Google Scholar 

  • Pascal P-Y, Dupuy C, Richard P, Mallet C, Armynot du Chatelet E, Niquil N (2009) Seasonal variation in consumption of benthic bacteria by meio- and macrofauna in an intertidal mudflat. Limnol Oceanogr 54:1048–1059

    Article  CAS  Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/.

  • Rieper M (1982) Feeding preferences of marine harpacticoid copepods for various species of bacteria. Mar Ecol Prog Ser 7:303–307

    Article  Google Scholar 

  • Rieper-Kirchner M (1990) Macroalgal decomposition: laboratory studies with particular regard to microorganisms and meiofauna. Helgol Meeresunters 44:397–410

    Article  Google Scholar 

  • Riera P, Hubas C (2003) Trophic ecology of nematodes from various microhabitats of the Roscoff Aber Bay (France): importance of stranded macroalgae evidenced through δ13C and δ15N. Mar Ecol Prog Ser 260:151–159

    Article  CAS  Google Scholar 

  • Riera P, Richard P (1996) Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine Bay of Marennes-Oléron. Estuar Coast Shelf Sci 42:347–360

    Article  Google Scholar 

  • Riera P, Richard P, Grémare A, Blanchard GF (1996) Food source of intertidal nematodes in the Bay of Marennes-Oléron (France), as determined by dual stable isotope analysis. Mar Ecol Prog Ser 142:303–309

    Article  CAS  Google Scholar 

  • Romeyn K, Bouwman LA (1983) Food selection and consumption by estuarine nematodes. Hydrobiol Bull 17:103–109

    Article  Google Scholar 

  • Rzeznik-Orignac J, Fichet D, Boucher G (2004) Extracting massive numbers of nematodes from muddy marine deposits: efficiency and selectivity. Nematology 6:605–616

    Article  Google Scholar 

  • Rzeznik-Orignac J, Boucher G, Fichet D, Richard P (2008) Stable isotope analysis of food source and trophic position of intertidal nematodes and copepods. Mar Ecol Prog Ser 359:145–150

    Article  Google Scholar 

  • Schaal G, Riera P, Leroux C (2008) Trophic coupling between two adjacent benthic food webs within a man-made intertidal area: a stable isotopes evidence. Estuar Coast Shelf Sci 77:523–534

    Article  Google Scholar 

  • Somerfield PJ, Warwick RM, Moens T (2005) Meiofauna techniques. In: Eleftheriou A, McIntyre A (eds) Methods for the study of marine benthos, 3rd edn. Blackwell science, Oxford, pp 229–272

    Chapter  Google Scholar 

  • Valentine JF, Duffy JE (2006) The central role of grazing in seagrass ecology. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 463–501

    Chapter  Google Scholar 

  • Valentine JF, Heck KL Jr (1999) Seagrass herbivory: evidence for the continued grazing of marine grasses. Mar Ecol Prog Ser 176:291–302

    Article  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web. Limnol Oceanogr 46:2061–2066

    Article  CAS  Google Scholar 

  • Vizzini S, Mazzola A (2003) Seasonal variations in the stable carbon and nitrogen isotope ratios (13C/12C and 15N/14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Mar Biol 142:1009–1018

    CAS  Google Scholar 

  • Vizzini S, Sarà G, Michener RH, Mazzola A (2002) The role and contribution of the seagrass Posidonia oceanica (L.) Delile organic matter for secondary consumers as revealed by carbon and nitrogen stable isotope analysis. Acta Oecol 23:277–285

    Article  Google Scholar 

  • Weber N (2003) De La Rochelle à la Pointe de la Coubre : Ile d’Oléron. Map no 7405G. SHOM, Brest

  • Wieser W (1953) Die beziehungen zwischen Mundhölengestalt, ernährungsweise und vorkommen bei freilebenden marinen nematoden. Ein ökologisch- morphhlogische studie. Ark Zool 4:439–484

    Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Pearson Education, Upper Saddle river

    Google Scholar 

Download references

Acknowledgments

This study is part of B. Lebreton’s Ph.D. thesis, which was supported by the French Ministry for Higher Education and Research, and participated to the MARBEF FoodWebio and COMPECO projects. Funding was also obtained through the research programs ‘ACI Ecologie Quantitative’ and ‘Programme National d’Environnement Côtier’, and the Poitou–Charentes Region programme CPER 2007–2013. The authors thank M. Bréret, F. Mornet, P. Pineau, T. Guyot, J. Pigeot, D. Vilday for their help during field work and C. Pfléger for her help in sample preparations, as well as the staff at the ‘Réserve naturelle nationale de Moëze-Oléron’. B. Lebreton is grateful to L. Hutchison for language corrections and to the 4 anonymous referees, which comments greatly improved earlier manuscript drafts.

Author information

Authors and Affiliations

  1. Littoral, Environnement et Sociétés (LIENSs), Institut du Littoral et de l’Environnement, UMR 7266 CNRS-Université de La Rochelle, 2 rue Olympe de Gouges, 17000, La Rochelle, France

    Benoit Lebreton, Pierre Richard, Robert Galois, Gilles Radenac, Amel Brahmia, Géraldine Colli, Marig Grouazel, Cyril André, Gaël Guillou & Gérard F. Blanchard

Authors
  1. Benoit Lebreton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pierre Richard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert Galois
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gilles Radenac
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Amel Brahmia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Géraldine Colli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marig Grouazel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Cyril André
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gaël Guillou
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gérard F. Blanchard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benoit Lebreton.

Additional information

Communicated by U. Sommer.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lebreton, B., Richard, P., Galois, R. et al. Food sources used by sediment meiofauna in an intertidal Zostera noltii seagrass bed: a seasonal stable isotope study. Mar Biol 159, 1537–1550 (2012). https://doi.org/10.1007/s00227-012-1940-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-012-1940-7

Keywords

  • Food Source
  • Microalgae
  • Credibility Interval
  • Meiofauna
  • Harpacticoid Copepod